Dietary conjugated linoleic acid activates PPARγ and the intestinal trefoil factor in SW480 cells and mice with dextran sulfate sodium-induced colitis

Journal of Nutrition

Volumn 142, Issue 12, 2012, Pages 2135-2140

  Borniquel, Sara ^a   Jädert, Cecilia ^a   Lundberg, Jon O ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

2 CHLORO 5 NITROBENZANILIDE; CONJUGATED LINOLEIC ACID; DEXTRAN SULFATE; HEME OXYGENASE 1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTESTINAL TREFOIL FACTOR; LINOLEIC ACID; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; COLITIS; CONTROLLED STUDY; DISEASE ACTIVITY; ENTERITIS; FEMALE; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; PROTECTION; PROTEIN DOMAIN; PROTEIN EXPRESSION; TREATMENT DURATION; UPREGULATION;

ANIMALS; ANTI-INFLAMMATORY AGENTS; COLITIS; DEXTRAN SULFATE; FEMALE; HEME OXYGENASE-1; INFLAMMATORY BOWEL DISEASES; LINOLEIC ACIDS, CONJUGATED; MEMBRANE PROTEINS; MICE; MICE, INBRED BALB C; MUCINS; PPAR GAMMA;

LOTUS; MUS;

EID: 84872129507     PISSN: 00223166     EISSN: 15416100     Source Type: Journal    
DOI: 10.3945/jn.112.163931     Document Type: Article

References (52)

1. McGuckin MA, Eri R, Simms LA, Florin TH, Radford-Smith G. Intestinal barrier dysfunction in inflammatory bowel diseases. Inflamm Bowel Dis. 2009;15:100-13.
2. Okayasu I, Hatakeyama S, Yamada M, Ohkusa T, Inagaki Y, Nakaya R. A novel method in the induction of reliable experimental acute and chronic ulcerative colitis in mice. Gastroenterology. 1990;98: 694-702.
3. Shirazi T, Longman RJ, Corfield AP, Probert CS. Mucins and inflammatory bowel disease. Postgrad Med J. 2000;76:473-8.
4. Van der Sluis M, De Koning BA, De Bruijn AC, Velcich A, Meijerink JP, Van Goudoever JB, Buller HA, Dekker J, Van Seuningen I, Renes IB, et al. Muc2-deficient mice spontaneously develop colitis, indicating that MUC2 is critical for colonic protection. Gastroenterology. 2006;131:117-29.
5. Petersson J, Schreiber O, Hansson GC, Gendler SJ, Velcich A, Lundberg JO, Roos S, Holm L, Phillipson M. Importance and regulation of the colonic mucus barrier in a mouse model of colitis. Am J Physiol Gastrointest Liver Physiol. 2011;300:G327-33.
6. Taupin D, Podolsky DK. Trefoil factors: initiators of mucosal healing. Nat Rev Mol Cell Biol. 2003;4:721-32.
7. Mashimo H, Wu DC, Podolsky DK, Fishman MC. Impaired defense of intestinal mucosa in mice lacking intestinal trefoil factor. Science. 1996;274:262-5.
8. Bassaganya-Riera J, Hontecillas R, Beitz DC. Colonic anti-inflammatory mechanisms of conjugated linoleic acid. Clin Nutr. 2002;21:451-9.
9. Kim DI, Kim KH, Kang JH, Jung EM, Kim SS, Jeung EB, Yang MP. Trans-10, cis-12-conjugated linoleic acid modulates NF-kappaB activation and TNF-alpha production in porcine peripheral blood mononuclear cells via a PPARgamma-dependent pathway. Br J Nutr. 2011;105:1329-36.
10. Cui T, Schopfer FJ, Zhang J, Chen K, Ichikawa T, Baker PR, Batthyany C, Chacko BK, Feng X, Patel RP, et al. Nitrated fatty acids: endogenous anti-inflammatory signaling mediators. J Biol Chem. 2006;281:35686-98.
11. Green S, Wahli W. Peroxisome proliferator-activated receptors: finding the orphan a home. Mol Cell Endocrinol. 1994;100:149-53.
12. Thompson EA. PPARgamma physiology and pathology in gastrointestinal epithelial cells. Mol Cells. 2007;24:167-76.
13. Katayama K, Wada K, Nakajima A, Mizuguchi H, Hayakawa T, Nakagawa S, Kadowaki T, Nagai R, Kamisaki Y, Blumberg RS, et al. A novel PPAR gamma gene therapy to control inflammation associated with inflammatory bowel disease in a murine model. Gastroenterology. 2003;124:1315-24.
14. Saubermann LJ, Nakajima A, Wada K, Zhao S, Terauchi Y, Kadowaki T, Aburatani H, Matsuhashi N, Nagai R, Blumberg RS. Peroxisome proliferator-activated receptor gamma agonist ligands stimulate a Th2 cytokine response and prevent acute colitis. Inflamm Bowel Dis. 2002; 8:330-9.
15. Su CGLazar MA, Wu GD. A novel therapy for colitis utilizing PPAR-gamma ligands to inhibit the epithelial inflammatory response. J Clin Invest. 1999;104:383-9.
16. Lytle C, Tod TJ, Vo KT, Lee JW, Atkinson RD, Straus DS. The peroxisome proliferator-activated receptor gamma ligand rosiglitazone delays the onset of inflammatory bowel disease in mice with interleukin 10 deficiency. Inflamm Bowel Dis. 2005;11:231-43.
17. Bassaganya-Riera J, Reynolds K, Martino-Catt S, Cui Y, Hennighausen L, Gonzalez F, Rohrer J, Benninghoff AU, Hontecillas R. Activation of PPAR gamma and delta by conjugated linoleic acid mediates protection from experimental inflammatory bowel disease. Gastroenterology. 2004;127:777-91.
18. Bassaganya-Riera J, Hontecillas R. CLA and n-3 PUFA differentially modulate clinical activity and colonic PPAR-responsive gene expression in a pig model of experimental IBD. Clin Nutr. 2006;25:454-65.
19. Shimada T, Fujii Y, Koike T, Tabei K, Namatame T, Yamagata M, Tajima A, Yoneda M, Terano A, Hiraishi H. Peroxisome proliferator-activated receptor gamma (PPARgamma) regulates trefoil factor family 2 (TFF2) expression in gastric epithelial cells. Int J Biochem Cell Biol. 2007;39:626-37.
20. Ito R, Shin-Ya M, Kishida T, Urano A, Takada R, Sakagami J, Imanishi J, Kita M, Ueda Y, Iwakura Y, et al. Interferon-gamma is causatively involved in experimental inflammatory bowel disease in mice. Clin Exp Immunol. 2006;146:330-8.
21. Borniquel S, Jansson EA, Cole MP, Freeman BA, Lundberg JO. Nitrated oleic acid up-regulates PPARgamma and attenuates experimental inflammatory bowel disease. Free Radic Biol Med. 2010;48:499-505.
22. Rousseaux C, Lefebvre B, Dubuquoy L, Lefebvre P, Romano O, Auwerx J, Metzger D, Wahli W, Desvergne B, Naccari GC, et al. Intestinal antiinflammatory effect of 5-aminosalicylic acid is dependent on peroxisome proliferator-activated receptor-gamma. J Exp Med. 2005; 201:1205-15.
23. Diaz-Granados N, Howe K, Lu J, McKay DM. Dextran sulfate sodium-induced colonic histopathology, but not altered epithelial ion transport, is reduced by inhibition of phosphodiesterase activity. Am J Pathol. 2000;156:2169-77.
24. Podolsky DK. The current future understanding of inflammatory bowel disease. Best Pract Res Clin Gastroenterol. 2002;16:933-43.
25. An G, Wei B, Xia B, McDaniel JM, Ju T, Cummings RD, Braun J, Xia L. Increased susceptibility to colitis and colorectal tumors in mice lacking core 3-derived O-glycans. J Exp Med. 2007;204:1417-29.
26. Podolsky DK. Inflammatory bowel disease. N Engl J Med. 2002;347:417-29.
27. Calder PC. Polyunsaturated fatty acids, inflammatory processes and inflammatory bowel diseases. Mol Nutr Food Res. 2008;52:885-97.
28. Belluzzi A. Polyunsaturated fatty acids (n-3 PUFAs) and inflammatory bowel disease (IBD): pathogenesis and treatment. Eur Rev Med Pharmacol Sci. 2004;8:225-9.
29. Bassaganya-Riera J, Hontecillas R. Dietary conjugated linoleic acid and n-3 polyunsaturated fatty acids in inflammatory bowel disease. Curr Opin Clin Nutr Metab Care. 2010;13:569-73.
30. Evans NP, Misyak SA, Schmelz EM, Guri AJ, Hontecillas R, Bassaganya-Riera J. Conjugated linoleic acid ameliorates inflammation-induced colorectal cancer in mice through activation of PPARgamma. J Nutr. 2010;140:515-21.
31. Shores DR, Binion DG, Freeman BA, Baker PR. New insights into the role of fatty acids in the pathogenesis and resolution of inflammatory bowel disease. Inflamm Bowel Dis. 2011;17:2192-204.
32. Badinga L, Greene ES. Physiological properties of conjugated linoleic acid and implications for human health. Nutr Clin Pract. 2006;21: 367-73.
33. Reynolds CM, Roche HM. Conjugated linoleic acid and inflammatory cell signalling. Prostaglandins Leukot Essent Fatty Acids. 2010;82: 199-204.
34. Calder PC. Immunoregulatory and anti-inflammatory effects of n-3 polyunsaturated fatty acids. Braz J Med Biol Res. 1998;31:467-90.
35. Calder PC. Dietary fatty acids and the immune system. Nutr Rev. 1998;56:S70-83.
36. Diep QN, Touyz RM, Schiffrin EL. Docosahexaenoic acid, a peroxi-some proliferator-activated receptor-alpha ligand, induces apoptosis in vascular smooth muscle cells by stimulation of p38 mitogen-activated protein kinase. Hypertension. 2000;36:851-5.
37. Nguyen KA, Carbone JM, Silva VM, Chen C, Hennig GE, Whiteley HE, Manautou JE. The PPAR activator docosahexaenoic acid prevents acetaminophen hepatotoxicity in male CD-1 mice. J Toxicol Environ Health A. 1999;58:171-86.
38. Hwang D. Fatty acids and immune responses: a new perspective in searching for clues to mechanism. Annu Rev Nutr. 2000;20:431-56.
39. Hontecillas R, Wannemeulher MJ, Zimmerman DR, Hutto DL, Wilson JH, Ahn DU, Bassaganya-Riera J. Nutritional regulation of porcine bacterial-induced colitis by conjugated linoleic acid. J Nutr. 2002; 132:2019-27.
40. Sarraf P, Mueller E, Jones D, King FJ, DeAngelo DJ, Partridge JB, Holden SA, Chen LB, Singer S, Fletcher C, et al. Differentiation and reversal of malignant changes in colon cancer through PPARgamma. Nat Med. 1998;4:1046-52.
41. Dubuquoy L, Rousseaux C, Thuru X, Peyrin-Biroulet L, Romano O, Chavatte P, Chamaillard M, Desreumaux P. PPARgamma as a new therapeutic target in inflammatory bowel diseases. Gut. 2006;55:1341-9.
42. Whigham LD, Watras AC, Schoeller DA. Efficacy of conjugated linoleic acid for reducing fat mass: a meta-analysis in humans. Am J Clin Nutr. 2007;85:1203-11.
43. Tenhunen R, Marver HS, Schmid R. The enzymatic conversion of heme to bilirubin by microsomal heme oxygenase. Proc Natl Acad Sci USA. 1968;61:748-55.
44. Paul G, Bataille F, Obermeier F, Bock J, Klebl F, Strauch U, Lochbaum D, Rummele P, Farkas S, Schölmerich J, et al. Analysis of intestinal haem-oxygenase-1 (HO-1) in clinical and experimental colitis. Clin Exp Immunol. 2005;140:547-55.
45. Varga C, Laszlo F, Fritz P, Cavicchi M, Lamarque D, Horvath K, Posa A, Berko A, Whittle BJ. Modulation by heme and zinc protoporphyrin of colonic heme oxygenase-1 and experimental inflammatory bowel disease in the rat. Eur J Pharmacol. 2007;561:164-71.
46. Vijayan V, Mueller S, Baumgart-Vogt E, Immenschuh S. Heme oxygenase-1 as a therapeutic target in inflammatory disorders of the gastrointestinal tract. World J Gastroenterol. 2010;16:3112-9.
47. Naito Y, Takagi T, Uchiyama K, Yoshikawa T. Heme oxygenase-1: a novel therapeutic target for gastrointestinal diseases. J Clin Biochem Nutr. 2011;48:126-33.
48. Shimada T, Koitabashi A, Fujii Y, Hashimoto T, Hosaka K, Tabei K, Namatame T, Yoneda M, Hiraishi H, Terano A. PPARgamma mediates NSAIDs-induced upregulation of TFF2 expression in gastric epithelial cells. FEBS Lett. 2004;558:33-8.
49. Azarschab P, Al-Azzeh E, Kornberger W, Gott P. Aspirin promotes TFF2 gene activation in human gastric cancer cell lines. FEBS Lett. 2001; 488:206-10.
50. Tanaka T, Kohno H, Yoshitani S, Takashima S, Okumura A, Murakami A, Hosokawa M. Ligands for peroxisome proliferator-activated receptors alpha and gamma inhibit chemically induced colitis and formation of aberrant crypt foci in rats. Cancer Res. 2001;61:2424-8.
51. Marion-Letellier R, Butler M, Déchelotte P, Playford RJ, Ghosh S. Comparation of cytokine modulation by natural peroxisome proliferator-activated receptor g ligands with synthetic ligands in intestinal-like Caco-2 cells and human dendritic cells-potential for dietary modulation of peroxisome proliferator-activated receptor g in intestinal inflammation. Am J Clin Nutr. 2008;87:939-48.
52. Yu Y, Correll PH, Vanden Heuvel JP. Conjugated linoleic acid decreases production of pro-inflammatory products in macrophages: evidence for a PPARg-dependent mechanism. Biochim Biophys Acta. 2002;1581:89-99.